Skip to main content

Spatial analysis of stable isotope data to determine primary sources of nutrition for fish

Abstract

Carbon and nitrogen stable isotopes were used to determine the ultimate autotrophic sources supporting production of three commercially important fish species over unvegetated mudflats in a subtropical estuary. Mean isotope values over the whole estuary for fish and autotroph sources were modeled to indicate feasible combinations of sources. Variability in isotope values among nine locations (separated by 3–10 km) was then used as a further test of the likelihood that sources were involved in fish nutrition. A positive spatial correlation between isotope values of a fish species and an autotroph indicates a substantial contribution from the autotroph. Spatial correlations were tested with a newly developed randomization procedure using differences between fish and autotroph values at each location, based on carbon and nitrogen isotopes combined in two-dimensional space. Both whole estuary modeling and spatial analysis showed that seagrass, epiphytic algae and particulate organic matter in the water column, including phytoplankton, are likely contributors to bream (Acanthopagrus australis) nutrition. However, spatial analysis also showed that mangroves were involved (up to 33% contribution), despite a very low contribution from whole estuary modeling. Spatial analysis on sand whiting (Sillago ciliata) demonstrated the importance of two sources, mangroves (up to 25%) and microalgae on the mudflats, considered unimportant based on whole estuary modeling. No spatial correlations were found between winter whiting (Sillago maculata) and autotrophs, either because fish moved among locations or relied on different autotrophs at different locations. Spatial correlations between consumer and source isotope values provide a useful analytical tool for identifying the role of autotrophs in foodwebs, and demonstrated here that both in situ production of microalgae and organic matter from adjacent habitats were important to fish over mudflats.

This is a preview of subscription content, access via your institution.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

References

  1. Adams TS, Sterner RW (2000) The effect of dietary nitrogen content on trophic level 15N enrichment. Limnol Oceanogr 45:601–607

    CAS  Google Scholar 

  2. Beaudoin CP, Tonn WM, Prepas EE, Wassenaar LI (1999) Individual specialisation and trophic adaptability of northern pike (Exos lucius): an isotope and dietary analysis. Oecologia 120:386–396

    Article  Google Scholar 

  3. Beck MW, Heck KL, Able KW, Childers DL, Eggleston DB, Gillanders BM, Halpern B, Hays CG, Hoshino K, Minello TJ, Orth RJ, Sheridan PF, Weinstein MR (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience 51:633–641

    Google Scholar 

  4. Boon PI, Bunn SE (1994) Variations in the stable isotope composition of aquatic plants and their implications for food web analysis. Aquat Bot 48:99–108

    Google Scholar 

  5. Boon PI, Bird FL, Bunn SE (1997) Diet of the intertidal callianassid shrimps Biffarius arenosus and Trypea australiensis (Decapoda: Thalassinidea) in Western Port (southern Australia), determined with multiple stable-isotope analyses. Mar Freshw Res 48:503–511

    CAS  Google Scholar 

  6. Bouillon S, Koedam N, Raman AV, Dehairs F (2002) Primary producers sustaining macro-invertebrate communities in intertidal mangrove forests. Oecologia 130:441–448

    Article  Google Scholar 

  7. Branstrator DK, Cabana G, Mazumder A, Rasmussen JB (2000) Measuring life-history omnivory in the opossum shrimp, Mysis relicta, with stable nitrogen isotopes. Limnol Oceanogr 45:463–467

    CAS  Google Scholar 

  8. Burchmore JJ, Pollard DA, Middleton MJ, Bell JD, Pease BC (1988) Biology of four species of whiting (Pisces: Sillaginidae) in Botany Bay, New South Wales. Aust J Mar Freshw Res 39:709–727

    Google Scholar 

  9. Chong VC, Low CB, Ichikawa T (2001) Contribution of mangrove detritus to juvenile prawn nutrition: a dual stable isotope study in a Malaysian mangrove forest. Mar Biol 138:77–86

    Article  CAS  Google Scholar 

  10. De Niro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351

    CAS  Google Scholar 

  11. Deegan LA, Garritt RH (1997) Evidence for spatial variability in estuarine food webs. Mar Ecol Prog Ser 147:31–47

    Google Scholar 

  12. Dennison WC, Abal EG (1999) Moreton Bay study: a scientific basis for the Healthy Waterways Campaign. South East Queensland Regional Water Quality Management Strategy, Brisbane

    Google Scholar 

  13. Fry B (1984) 13C/12C ratios and the trophic importance of algae in Florida Syringodium filiforme seagrass meadows. Mar Biol 79:11–19

    CAS  Google Scholar 

  14. Fry B, Macko SA, Zieman JC (1986) Review of stable isotopic investigations of food webs in seagrass meadows. Fla Mar Res Pub 42:189–209

    Google Scholar 

  15. Gee JM (1989) An ecological and economic review of meiofauna as food for fish. Zool J Linn Soc 96:243–261

    Google Scholar 

  16. Harrigan P, Zieman JC, Macko SA (1989) The base of nutritional support for the gray snapper (Lutjanus griseus): an evaluation based on a combined stomach content and stable isotope analysis. Bull Mar Sci 44:65–77

    Google Scholar 

  17. Herman PMJ, Middelburg JJ, Widdows J, Lucas CH, Heip CHR (2000) Stable isotopes as trophic tracers: combining field sampling and manipulative labelling of food resources for macrobenthos. Mar Ecol Prog Ser 204:79–92

    CAS  Google Scholar 

  18. Hesslein RH, Hallard KA, Ramlal P (1993) Replacement of sulphur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by d34S, d13C, and d15N. Can J Fish Aquat Sci 50:2071–2076

    CAS  Google Scholar 

  19. Kerby BM, Brown IW (1994) Bream, whiting and flathead in southeast Queensland: a review of the literature. Department of Primary Industries, Brisbane

  20. Kitting CL, Fry B, Morgan MD (1984) Detection of inconspicuous epiphytic algae supporting food webs in seagrass meadows. Oecologia 62:145–149

    Google Scholar 

  21. Kneib R (2000) Saltmarsh ecoscapes and production transfer by estuarine nekton in the southeastern United States. In: Weinstein MP, Kreeger DA (eds) Concepts and controversies in tidal marsh ecology. Kluwer, Dordrecht

  22. Lee SY (1995) Mangrove outwelling: a review. Hydrobiologia 295:203–212

    Google Scholar 

  23. Loneragan NR, Bunn SE, Kellaway DM (1997) Are mangroves and seagrasses sources of organic carbon for penaeid prawns in a tropical Australian estuary? A multiple stable isotope study. Mar Biol 130:289–300

    Article  Google Scholar 

  24. McCutchan JH, Lewis WM (2002) Relative importance of carbon sources for macroinvertebrates in a Rocky Mountain stream. Limnol Oceanogr 47:742–752

    Google Scholar 

  25. Michener RH, Schell DM (1994) Stable isotope ratios as tracers in marine aquatic food webs. In: Lajtha K, Michener RH (eds) Stable isotopes in ecology and environmental science. Blackwell, Oxford, pp 138–157

  26. Middelburg JJ, Barranguet C, Boschker HTS, Herman PMJ, Moens T, Heip CHR (2000) The fate of intertidal microphytobenthos carbon: An in situ 13C-labeling study. Limnol Oceanogr 45:1224–1234

    CAS  Google Scholar 

  27. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140

    CAS  Google Scholar 

  28. Moncrieff CA, Sullivan MJ (2001) Trophic importance of epiphytic algae in subtropical seagrass beds: evidence from multiple stable isotope analysis. Mar Ecol Prog Ser 215:93–106

    Google Scholar 

  29. Morton RM, Pollock BR, Beumer JP (1987) The occurrence and diet of fishes in a tidal inlet to a saltmarsh in southern Moreton Bay, Queensland. Aust J Ecol 12:217–237

    Google Scholar 

  30. Nichols PD, Klumpp DW, Johns RB (1985) A study of food chains in seagrass communities III. Stable carbon isotope ratios. Aust J Mar Freshw Res 36:683–690

    CAS  Google Scholar 

  31. Odum EP (1984) The status of three ecosystem-level hypotheses regarding salt marsh estuaries: tidal subsidy, outwelling and detritus-based food chains. In: Kennedy VS (ed) Estuarine perspectives. Academic Press, New York, pp 485–495

  32. Ogawa N, Ogura N (1997) Dynamics of particulate organic matter in the Tamagawa Estuary and inner Tokyo Bay. Estuar Coast Shelf Sci 44:263–273

    Article  CAS  Google Scholar 

  33. Overman NC, Parrish DL (2001) Stable isotope composition of walleye: 15N accumulation with age and area-specific differences in d13C. Can J Fish Aquat Sci 58:1253–1260

    Article  Google Scholar 

  34. Peterson BJ (1999) Stable isotopes as tracers of organic matter input and transfer in benthic food webs: a review. Acta Oecol 20:479–487

    Article  Google Scholar 

  35. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  36. Peterson BJ, Howarth RW, Garritt RH (1986) Sulfur and carbon isotopes as tracers of salt-marsh organic matter flow. Ecology 67:865–874

    CAS  Google Scholar 

  37. Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179

    Article  Google Scholar 

  38. Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia (in press)

    Google Scholar 

  39. Rau GH, Ralston S, Southon JR, Chavez FP (2001) Upwelling and the condition and diet of juvenile rockfish: a study using 14C, 13C, and 15N natural abundances. Limnol Oceanogr 46:1565–1570

    CAS  Google Scholar 

  40. Rodelli MR, Gearing JN, Gearing PJ, Marshall N, Sasekumar A (1984) Stable isotope ratio as a tracer of mangrove carbon in Malaysian ecosystems. Oecologia 61:326–333

    Google Scholar 

  41. Stephenson RL, Tan FC, Mann KH (1984) Stable carbon isotope variability in marine macrophytes and its implications for food web studies. Mar Biol 81:223–230

    CAS  Google Scholar 

  42. Sullivan MJ, Moncrieff CA (1990) Edaphic algae are an important component of salt marsh food-webs: evidence from multiple stable isotope analyses. Mar Ecol Prog Ser 62:149–159

    Google Scholar 

  43. Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066

    Google Scholar 

Download references

Acknowledgments

We thank G. Mount and B. Thomas for field assistance, K. Preston for processing microalgae samples, and T. Gaston for comments on the manuscript. This project was supported by a Fisheries Research and Development Corporation grant to R.M.C.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Rod M. Connolly.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Melville, A.J., Connolly, R.M. Spatial analysis of stable isotope data to determine primary sources of nutrition for fish. Oecologia 136, 499–507 (2003). https://doi.org/10.1007/s00442-003-1302-8

Download citation

Keywords

  • Estuary
  • Mangroves
  • Microphytobenthos
  • Seagrass
  • Spatial variability